Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies
Cardiomyocytes generated from induced pluripotent cells hold great promise for understanding and treating heart disease. William Pu and his colleagues apply new technologies for studying such cardiomyocytes from patients with Barth syndrome to explore how the mitochondrial defects characteristic of...
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| Published in | Nature medicine Vol. 20; no. 6; pp. 616 - 623 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.06.2014
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1078-8956 1546-170X 1546-170X |
| DOI | 10.1038/nm.3545 |
Cover
| Abstract | Cardiomyocytes generated from induced pluripotent cells hold great promise for understanding and treating heart disease. William Pu and his colleagues apply new technologies for studying such cardiomyocytes from patients with Barth syndrome to explore how the mitochondrial defects characteristic of this syndrome lead to heart dysfunction.
Study of monogenic mitochondrial cardiomyopathies may yield insights into mitochondrial roles in cardiac development and disease. Here, we combined patient-derived and genetically engineered induced pluripotent stem cells (iPSCs) with tissue engineering to elucidate the pathophysiology underlying the cardiomyopathy of Barth syndrome (BTHS), a mitochondrial disorder caused by mutation of the gene encoding tafazzin (
TAZ
). Using BTHS iPSC-derived cardiomyocytes (iPSC-CMs), we defined metabolic, structural and functional abnormalities associated with
TAZ
mutation. BTHS iPSC-CMs assembled sparse and irregular sarcomeres, and engineered BTHS 'heart-on-chip' tissues contracted weakly. Gene replacement and genome editing demonstrated that
TAZ
mutation is necessary and sufficient for these phenotypes. Sarcomere assembly and myocardial contraction abnormalities occurred in the context of normal whole-cell ATP levels. Excess levels of reactive oxygen species mechanistically linked
TAZ
mutation to impaired cardiomyocyte function. Our study provides new insights into the pathogenesis of Barth syndrome, suggests new treatment strategies and advances iPSC-based
in vitro
modeling of cardiomyopathy. |
|---|---|
| AbstractList | Study of monogenic mitochondrial cardiomyopathies may yield insights into mitochondrial roles in cardiac development and disease. Here, we combined patient-derived and genetically engineered induced pluripotent stem cells (iPSCs) with tissue engineering to elucidate the pathophysiology underlying the cardiomyopathy of Barth syndrome (BTHS), a mitochondrial disorder caused by mutation of the gene encoding tafazzin (TAZ). Using BTHS iPSC-derived cardiomyocytes (iPSC-CMs), we defined metabolic, structural and functional abnormalities associated with TAZ mutation. BTHS iPSC-CMs assembled sparse and irregular sarcomeres, and engineered BTHS 'heart-on-chip' tissues contracted weakly. Gene replacement and genome editing demonstrated that TAZ mutation is necessary and sufficient for these phenotypes. Sarcomere assembly and myocardial contraction abnormalities occurred in the context of normal whole-cell ATP levels. Excess levels of reactive oxygen species mechanistically linked TAZ mutation to impaired cardiomyocyte function. Our study provides new insights into the pathogenesis of Barth syndrome, suggests new treatment strategies and advances iPSC-based in vitro modeling of cardiomyopathy. Study of monogenic mitochondrial cardiomyopathies may yield insights into mitochondrial roles in cardiac development and disease. Here, we combined patient-derived and genetically engineered induced pluripotent stem cells (iPSCs) with tissue engineering to elucidate the pathophysiology underlying the cardiomyopathy of Barth syndrome (BTHS), a mitochondrial disorder caused by mutation of the gene encoding tafazzin (TAZ). Using BTHS iPSC-derived cardiomyocytes (iPSC-CMs), we defined metabolic, structural and functional abnormalities associated with TAZ mutation. BTHS iPSC-CMs assembled sparse and irregular sarcomeres, and engineered BTHS 'heart-on-chip' tissues contracted weakly. Gene replacement and genome editing demonstrated that TAZ mutation is necessary and sufficient for these phenotypes. Sarcomere assembly and myocardial contraction abnormalities occurred in the context of normal whole-cell ATP levels. Excess levels of reactive oxygen species mechanistically linked TAZ mutation to impaired cardiomyocyte function. Our study provides new insights into the pathogenesis of Barth syndrome, suggests new treatment strategies and advances iPSC-based in vitro modeling of cardiomyopathy.Study of monogenic mitochondrial cardiomyopathies may yield insights into mitochondrial roles in cardiac development and disease. Here, we combined patient-derived and genetically engineered induced pluripotent stem cells (iPSCs) with tissue engineering to elucidate the pathophysiology underlying the cardiomyopathy of Barth syndrome (BTHS), a mitochondrial disorder caused by mutation of the gene encoding tafazzin (TAZ). Using BTHS iPSC-derived cardiomyocytes (iPSC-CMs), we defined metabolic, structural and functional abnormalities associated with TAZ mutation. BTHS iPSC-CMs assembled sparse and irregular sarcomeres, and engineered BTHS 'heart-on-chip' tissues contracted weakly. Gene replacement and genome editing demonstrated that TAZ mutation is necessary and sufficient for these phenotypes. Sarcomere assembly and myocardial contraction abnormalities occurred in the context of normal whole-cell ATP levels. Excess levels of reactive oxygen species mechanistically linked TAZ mutation to impaired cardiomyocyte function. Our study provides new insights into the pathogenesis of Barth syndrome, suggests new treatment strategies and advances iPSC-based in vitro modeling of cardiomyopathy. Cardiomyocytes generated from induced pluripotent cells hold great promise for understanding and treating heart disease. William Pu and his colleagues apply new technologies for studying such cardiomyocytes from patients with Barth syndrome to explore how the mitochondrial defects characteristic of this syndrome lead to heart dysfunction. Study of monogenic mitochondrial cardiomyopathies may yield insights into mitochondrial roles in cardiac development and disease. Here, we combined patient-derived and genetically engineered induced pluripotent stem cells (iPSCs) with tissue engineering to elucidate the pathophysiology underlying the cardiomyopathy of Barth syndrome (BTHS), a mitochondrial disorder caused by mutation of the gene encoding tafazzin ( TAZ ). Using BTHS iPSC-derived cardiomyocytes (iPSC-CMs), we defined metabolic, structural and functional abnormalities associated with TAZ mutation. BTHS iPSC-CMs assembled sparse and irregular sarcomeres, and engineered BTHS 'heart-on-chip' tissues contracted weakly. Gene replacement and genome editing demonstrated that TAZ mutation is necessary and sufficient for these phenotypes. Sarcomere assembly and myocardial contraction abnormalities occurred in the context of normal whole-cell ATP levels. Excess levels of reactive oxygen species mechanistically linked TAZ mutation to impaired cardiomyocyte function. Our study provides new insights into the pathogenesis of Barth syndrome, suggests new treatment strategies and advances iPSC-based in vitro modeling of cardiomyopathy. |
| Audience | Academic |
| Author | Li, Kai Pu, William T Roberts, Amy E Murry, Charles E He, Aibin Chien, Kenneth R Kulik, Wim Wang, Gang Wanders, Ronald J A Wang, Da-Zhi McCain, Megan L Yuan, Hongyan Laflamme, Michael A Zhang, Donghui Wang, Jiwu Pasqualini, Francesco Silvio Church, George M Geva, Judith Ma, Qing Ding, Jian Kelley, Richard I Vaz, Frédéric M Chen, Jinghai Parker, Kevin Kit Jiang, Dawei Zangi, Lior Yang, Luhan Agarwal, Ashutosh |
| Author_xml | – sequence: 1 givenname: Gang surname: Wang fullname: Wang, Gang organization: Department of Cardiology, Boston Children's Hospital – sequence: 2 givenname: Megan L surname: McCain fullname: McCain, Megan L organization: Wyss Institute for Biologically Inspired Engineering, School of Engineering and Applied Sciences, Harvard University – sequence: 3 givenname: Luhan surname: Yang fullname: Yang, Luhan organization: Wyss Institute for Biologically Inspired Engineering, School of Engineering and Applied Sciences, Harvard University, Department of Genetics, Harvard Medical School – sequence: 4 givenname: Aibin surname: He fullname: He, Aibin organization: Department of Cardiology, Boston Children's Hospital – sequence: 5 givenname: Francesco Silvio orcidid: 0000-0001-7038-3121 surname: Pasqualini fullname: Pasqualini, Francesco Silvio organization: Wyss Institute for Biologically Inspired Engineering, School of Engineering and Applied Sciences, Harvard University – sequence: 6 givenname: Ashutosh surname: Agarwal fullname: Agarwal, Ashutosh organization: Wyss Institute for Biologically Inspired Engineering, School of Engineering and Applied Sciences, Harvard University – sequence: 7 givenname: Hongyan surname: Yuan fullname: Yuan, Hongyan organization: Wyss Institute for Biologically Inspired Engineering, School of Engineering and Applied Sciences, Harvard University – sequence: 8 givenname: Dawei surname: Jiang fullname: Jiang, Dawei organization: Department of Cardiology, Boston Children's Hospital – sequence: 9 givenname: Donghui surname: Zhang fullname: Zhang, Donghui organization: Department of Cardiology, Boston Children's Hospital – sequence: 10 givenname: Lior surname: Zangi fullname: Zangi, Lior organization: Department of Cardiology, Boston Children's Hospital – sequence: 11 givenname: Judith surname: Geva fullname: Geva, Judith organization: Department of Cardiology, Boston Children's Hospital – sequence: 12 givenname: Amy E surname: Roberts fullname: Roberts, Amy E organization: Department of Cardiology, Boston Children's Hospital, Department of Medicine, Division of Genetics, Boston Children's Hospital – sequence: 13 givenname: Qing surname: Ma fullname: Ma, Qing organization: Department of Cardiology, Boston Children's Hospital – sequence: 14 givenname: Jian surname: Ding fullname: Ding, Jian organization: Department of Cardiology, Boston Children's Hospital – sequence: 15 givenname: Jinghai surname: Chen fullname: Chen, Jinghai organization: Department of Cardiology, Boston Children's Hospital – sequence: 16 givenname: Da-Zhi surname: Wang fullname: Wang, Da-Zhi organization: Department of Cardiology, Boston Children's Hospital – sequence: 17 givenname: Kai surname: Li fullname: Li, Kai organization: Department of Cardiology, Boston Children's Hospital – sequence: 18 givenname: Jiwu surname: Wang fullname: Wang, Jiwu organization: Allele Biotechnology & Pharmaceuticals, Inc., Department of Photobiology and Bioengineering, The Scintillon Institute – sequence: 19 givenname: Ronald J A surname: Wanders fullname: Wanders, Ronald J A organization: Department of Clinical Chemistry and Pediatrics, Laboratory of Genetic Metabolic Diseases, Academic Medical Center – sequence: 20 givenname: Wim surname: Kulik fullname: Kulik, Wim organization: Department of Clinical Chemistry and Pediatrics, Laboratory of Genetic Metabolic Diseases, Academic Medical Center – sequence: 21 givenname: Frédéric M surname: Vaz fullname: Vaz, Frédéric M organization: Department of Clinical Chemistry and Pediatrics, Laboratory of Genetic Metabolic Diseases, Academic Medical Center – sequence: 22 givenname: Michael A surname: Laflamme fullname: Laflamme, Michael A organization: Department of Pathology, Center for Cardiovascular Biology and Institute for Stem Cell and Regenerative Medicine, University of Washington – sequence: 23 givenname: Charles E surname: Murry fullname: Murry, Charles E organization: Department of Pathology, Center for Cardiovascular Biology and Institute for Stem Cell and Regenerative Medicine, University of Washington, Department of Bioengineering, Center for Cardiovascular Biology, Institute for Stem Cell and Regenerative Medicine, University of Washington, Department of Medicine and Cardiology, Center for Cardiovascular Biology, Institute for Stem Cell and Regenerative Medicine, University of Washington – sequence: 24 givenname: Kenneth R surname: Chien fullname: Chien, Kenneth R organization: Department of Cell and Molecular Biology and Medicine, Karolinska Institutet – sequence: 25 givenname: Richard I surname: Kelley fullname: Kelley, Richard I organization: Division of Metabolism, Kennedy Krieger Institute – sequence: 26 givenname: George M surname: Church fullname: Church, George M organization: Wyss Institute for Biologically Inspired Engineering, School of Engineering and Applied Sciences, Harvard University, Department of Genetics, Harvard Medical School – sequence: 27 givenname: Kevin Kit surname: Parker fullname: Parker, Kevin Kit email: kkparker@seas.harvard.edu organization: Wyss Institute for Biologically Inspired Engineering, School of Engineering and Applied Sciences, Harvard University, Harvard Stem Cell Institute, Harvard University – sequence: 28 givenname: William T surname: Pu fullname: Pu, William T email: wpu@enders.tch.harvard.edu organization: Department of Cardiology, Boston Children's Hospital, Harvard Stem Cell Institute, Harvard University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24813252$$D View this record in MEDLINE/PubMed http://kipublications.ki.se/Default.aspx?queryparsed=id:129149294$$DView record from Swedish Publication Index |
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| ContentType | Journal Article |
| Copyright | Springer Nature America, Inc. 2014 COPYRIGHT 2014 Nature Publishing Group Copyright Nature Publishing Group Jun 2014 |
| Copyright_xml | – notice: Springer Nature America, Inc. 2014 – notice: COPYRIGHT 2014 Nature Publishing Group – notice: Copyright Nature Publishing Group Jun 2014 |
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| Snippet | Cardiomyocytes generated from induced pluripotent cells hold great promise for understanding and treating heart disease. William Pu and his colleagues apply... Study of monogenic mitochondrial cardiomyopathies may yield insights into mitochondrial roles in cardiac development and disease. Here, we combined... |
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| SubjectTerms | 13/100 13/107 42/109 45/41 631/443/592/75/74 9/10 ATP Barth syndrome Barth Syndrome - genetics Barth Syndrome - physiopathology Biomedicine Cancer Research Cardiomyocytes Cardiomyopathy Cardiomyopathy, Dilated - genetics Cardiomyopathy, Dilated - physiopathology Cell Separation Complications and side effects Development and progression Genetic aspects Genetic disorders Heart diseases Humans Induced Pluripotent Stem Cells - physiology Infectious Diseases Magnetics Metabolic Diseases Mitochondrial Diseases - genetics Mitochondrial Diseases - physiopathology Models, Biological Molecular Medicine Mutation Myocardial Contraction - physiology Myocytes, Cardiac - physiology Neurosciences Pathogenesis Physiological aspects Reactive Oxygen Species - metabolism Risk factors Stem cells Tissue engineering Tissue Engineering - methods Transcription Factors - genetics |
| Title | Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies |
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